Telomeres protect chromosome ends from degradation and recombination events. For this reason, telomeres and telomerase, the enzyme that maintains telomere length homeostasis, are essential to genome integrity and are crucially implicated in tumorigenesis. The long noncoding RNA TERRA is transcribed from telomeres and represents a key component of telomere biology. However, the dynamics of TERRA transcripts and the mechanisms regulating TERRA expression are still poorly known. Interestingly, TERRA associates with telomerase in cancer cells, but its role in the regulation of telomerase remains unknown. We developed an in vivo approach to visualize and study endogenous TERRA molecules in living yeast cells. Our results indicate that TERRA transcripts organize telomerase activity at short telomeres by promoting formation of telomerase clusters and their subsequent relocation to the TERRA expressing telomere. We will use this approach to unveil the biology of TERRA in human cancer cells.